Abstract
Fermented foods provide novel ecological opportunities for natural populations of microbes to evolve through successive recolonization of resource-rich substrates. Comparative genomic data have reconstructed the evolutionary histories of microbes adapted to food environments, but experimental studies directly demonstrating the process of domestication are lacking for most fermented food microbes. Here, we show that during adaptation to cheese, phenotypic and metabolomic traits of wild Penicillium molds rapidly change to produce domesticated phenotypes with properties similar to those of the industrial cultures used to make Camembert and other bloomy rind cheeses. Over a period of just a few weeks, populations of wild Penicillium strains serially passaged on cheese had reduced pigment, spore, and mycotoxin production. Domesticated strains also had a striking change in volatile metabolite production, shifting from production of earthy or musty volatile compounds (e.g., geosmin) to fatty and cheesy volatiles (e.g., 2-nonanone, 2-undecanone). RNA sequencing demonstrated a significant decrease in expression of 356 genes in domesticated strains, with an enrichment of many secondary metabolite production pathways in these downregulated genes. By manipulating the presence of neighboring microbial species and overall resource availability, we demonstrate that the limited competition and high nutrient availability of the cheese environment promote rapid trait evolution of Penicillium molds.IMPORTANCE Industrial cultures of filamentous fungi are used to add unique aesthetics and flavors to cheeses and other microbial foods. How these microbes adapted to live in food environments is generally unknown as most microbial domestication is unintentional. Our work demonstrates that wild molds closely related to the starter culture Penicillium camemberti can readily lose traits and quickly shift toward producing desirable aroma compounds. In addition to experimentally demonstrating a putative domestication pathway for P. camemberti, our work suggests that wild Penicillium isolates could be rapidly domesticated to produce new flavors and aesthetics in fermented foods.
Highlights
Fermented foods provide novel ecological opportunities for natural populations of microbes to evolve through successive recolonization of resource-rich substrates
To experimentally evolve Penicillium on cheese, two non-starter Penicillium strains (Penicillium commune strain 162_3FA and Penicillium sp. strain 12) isolated from a cheese cave in Vermont in the United States were serially passaged on cheese curd agar (CCA) in the laboratory
To determine how competition from neighboring cheese microbes impacts the rate of phenotypic diversification, we serially passaged replicate populations alone (“Penicillium alone”) or in the presence of a mix of three competitors (“Penicillium ϩ community,” including the yeast Debaryomyces hansenii and the bacteria Brachybacterium alimentarium and Staphylococcus xylosus) that commonly cooccur with Penicillium species in cheese rinds [14, 16, 17]
Summary
Fermented foods provide novel ecological opportunities for natural populations of microbes to evolve through successive recolonization of resource-rich substrates. In addition to experimentally demonstrating a putative domestication pathway for P. camemberti, our work suggests that wild Penicillium isolates could be rapidly domesticated to produce new flavors and aesthetics in fermented foods Fermented foods such as cheese, miso, sourdough, and sauerkraut are hybrid microbiomes where wild microbial species from the environment mix with domesticated microbes that are added as starter cultures. The white surface of Camembert and Brie is created by a variety of strains of the starter culture P. camemberti This domesticated fungus is white, makes fewer conidia (asexual spores) than most wild Penicillium species, does not make detectable levels of mycotoxins, and produces desirable mushroom-like and fatty volatiles during cheese ripening [10,11,12] (Fig. 1A). Historical accounts suggest that white domesticated strains of Penicillium species were either directly isolated from French cheeses or produced in laboratories in France [13], but the potential domestication processes that generated these iconic cheese mold species have not been identified
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